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2014
Relationship Between Jaw Apparatus, Feeding
Habit, and Food Source in Oriental
Woodpeckers
Zoological Science, Tokyo, v. 31, n. 4, p. 223-227, 2014
http://www.producao.usp.br/handle/BDPI/45042
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Relationship Between Jaw Apparatus, Feeding Habit, and Food Source in
Oriental Woodpeckers
Author(s): Reginaldo José Donatelli , Elizabeth Höfling and Ana Luiza C. Catalano
Source: Zoological Science, 31(4):223-227. 2014.
Published By: Zoological Society of Japan
DOI: http://dx.doi.org/10.2108/zs130146
URL: http://www.bioone.org/doi/full/10.2108/zs130146
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ZOOLOGICAL SCIENCE 31: 223–227 (2014)
¤ 2014 Zoological Society of Japan
Relationship Between Jaw Apparatus, Feeding Habit, and Food
Source in Oriental Woodpeckers
Reginaldo José Donatelli1*, Elizabeth Höfling2, and Ana Luiza C. Catalano3
1
Laboratório de Ornitologia, Departamento de Ciências Biológicas, FC-UNESP, Caixa Postal 473,
17001-970, Bauru, SP, Brazil
2
Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo,
Rua do Matão Travessa 14, 101, 05508-090, São Paulo, Brazil
3
Programa de pós-graduação em Zoologia, Instituto de Biociências, Unesp,
campus de Botucatu, Cep, 18968-000, Botucatu, SP, Brazil
Associations among feeding habit, beak type, and food source in birds have been widely studied
and are well known to exist. The relationship between feeding habit and jaw apparatus in birds has
not attracted attention from ornithologists, perhaps because of the complexity of the skeletal morphology of the feeding system of birds. The goal of this study was to compare the jaw apparatus
and foraging strategies of various Oriental species of the Picidae (Meiglyptini and Picini tribes)
using a morphofunctional analysis of the skeletal structure of the jaw apparatus. This study showed
that there are at least three types of jaw apparatus in these woodpeckers, as follows: 1) robust,
developed, and complex; 2) complexity and development intermediate, as observed in Meiglyptes
tristis and Dinopium spp., whose main foraging method involves gleaning, probing, and tapping;
and 3) poorly developed, as observed in Picus miniaceus and Hemicircus concretus. The success
of woodpeckers as a natural group is due not only to their feeding diversity, but also their ability
to explore a wide range of different resources, as appropriate to their jaw apparatus.
Key words:
birds, Oriental Picidae, jaw apparatus, feeding habits, form and function
INTRODUCTION
In living organisms, the combination of form and function
creates relative stability and survival over time. Although the
two ideas of form and function are closely linked, they can
be conceptually distinguished from one another (Dullemeijer,
2001).
Associations among feeding habit, beak type, and food
source in birds have been universally studied and are well
known to exist. Studies about the role of skeletal structural
elements, cranial ligaments, and the functions of the maxillary musculature were conducted by Bock on various occasions (1960; 1964; 1966). However, the relationship between
feeding habit and jaw apparatus in birds has not drawn the
attention of ornithologists, perhaps because the skeletal elements of the feeding systems of birds are highly complex,
making morphological analyses challenging. Richards and
Bock (1973, p.78), who were aware of the lack of information about the relationship between form and function,
formed hypotheses about the relationship between feeding
strategy and jaw apparatus in the genus Loxops (Aves:
Drepanididae) that can be used as a reference for future
studies of other groups of birds.
Regarding the Picidae tribe, Bock (2001) states that
woodpeckers “have an interesting feeding apparatus con* Corresponding author. Tel. : +55-14-31036078;
Fax : +55-14-31036092;
E-mail: [email protected]
doi:10.2108/zs130146
sisting of two different parts – the bill for drilling into trees to
explore their prey and the tongue for capturing their prey.”
The question to be answered in this study is related to jaw
apparatus function. The behaviors and feeding specializations described for woodpeckers (Short, 1982), which are
associated with certain foraging strategies (Winkler et al.,
1995) and food sources (Winkler and Christie, 2002), may
or may not be related to variation in the form of the jaw
apparatus.
The aim of the present study was to examine the jaw
apparatus of various species of the Oriental woodpeckers
(Picidae: Meiglyptini and Picini tribes, sensu Winkler and
Christie, 2002) and, based on a morphofunctional analysis
of jaw structure, relate it to the foraging strategy. We
intended to answer the following questions: is there a relationship between foraging strategy and structure of the jaw
apparatus in the Oriental woodpeckers? Can a form-andfunction relationship be identified between structural characteristics of the jaw apparatus and foraging strategy?
MATERIALS AND METHODS
Material
The present study examined the cranial osteological and musculature characteristics that move the jaws of 15 Meiglyptini specimens, pertaining to six species and three genera, and 31 Picini
specimens, pertaining to 14 species and six genera. The materials
used in the study were from the collections of the National Museum
of Natural History (USNM), Smithsonian Institution, Washington
D.C., United States of America, and the Zoologicum Bogoriense
Museum, Indonesian Institute of Sciences (LIPI), Natural History
224
R. J. Donatelli et al.
Museum of the Indonesian Institute of Sciences (MZB), Indonesia.
The nomenclature of scientific names follows Winkler and Christie
(2002). Specimens with their museum abbreviations and numbers
of collections included in this study are as follows: (1) Meiglyptini –
Hemicircus concretus (Temminck, 1821) LIPI MZB.Skt 125 Hc1
and LIPI MZB.Skt 126 Hc2; Meiglyptes tristis (Horsfield, 1821) LIPI
MZB.Skt 123 Mtr1, MZB.Skt 124 Mtr2 and USNM 292228 ‫; ۅ‬
Meiglyptes tukki (Lesson, 1839) LIPI MZB.Skt 121 Mtu1, MZB.Skt
122 Mtk1 and USNM 489269 ‫ ; ۃ‬Mulleripicus pulverulentus
(Temminck, 1826) LIPI MZB.Skt 127 Mp1, MZB.Skt 128 Mp2,
USNM 19201 ‫ ۃ‬and USNM 562042 ‫ ; ۃ‬Mulleripicus fulvus (Quoy
and Gaimard, 1830) USNM 491227 ‫ ۃ‬and USNM 226191 ‫; ۃ‬
Mulleripicus funebris (Valenciennes, 1826) USNM 489265 ‫ ۅ‬. (2)
Picini - Reinwardtipicus validus (Temminck, 1825) LIPI MZB.Skt
119 Rv1; MZB.Skt 120 Rv2; Gecinulus viridis Blyth, 1862 USNM
620306 ‫ ; ۃ‬Blythipicus rubiginosus (Swainson, 1837) LIPI MZB.Skt
117 Br1; MZB.Skt 118 Br2; USNM 489267 ‫ ۃ‬, USNM 559840 ‫; ۃ‬
Chrysocolaptes lucidus (Scopoli, 1796) USNM 613082 ‫ ۅ‬, USNM
431475 ‫ ۅ‬, USNM 613081 ‫ ; ۅ‬Dinopium benghalense (Linnaeus,
1758) USNM 346830 ‫ ۃ‬, USNM 289692 ‫ ۃ‬, USNM 490202 ‫; ۅ‬
Dinopium javanense (Ljungh, 1797) LIPI MZB.Skt 115 Dij1; MZB.Skt
116 Dij2; USNM 318076 ‫ ۅ‬, USNM 318075 ‫ ۅ‬, USNM 562041 ‫; ۃ‬
Dinopium rafflesii (Vigors and Horsfield, 1830) LIPI MZB.Skt 114 Dr1;
Picus viridis Linnaeus, 1758 USNM 557540‫ ;ۅ‬Picus vittatus Vieillot,
1818 USNM 290962 ‫ ۃ‬, USNM 321099 ‫ ; ۅ‬Picus flavinucha Gould,
1834 USNM 620313 ‫ ; ۃ‬Picus canus Gmelin, 1788 USNM 289905
‫ ۅ‬, USNM 292049 ‫ ۅ‬, USNM 321598?; Picus mentalis Temminck,
1825 LIPI MZB.Skt 110 Pm1; MZB.Skt 110 Pm2; Picus miniaceus
Pennant, 1789 LIPI MZB.Skt. 112 Pmi3; Picus puniceus Horsfield,
1821 LIPI MZB.Skt 113 Pp2.
Methods
A complete anatomical description and details of the parts that
compose the jaw apparatus of the woodpecker species in this study
can be found in Donatelli (2012a, b, c, d).
Only the anatomical features most relevant to foraging are discussed in the present study. Furthermore, information about the foraging strategies (methods of obtaining food) of the Picidae species
was collected from a specialized literature (e.g., Short, 1982; Winkler
et al., 1995; Winkler and Christie, 2002). Definitions of woodpecker
foraging behaviors are presented in Winkler et al. (1995), with additional suggestions in Remsen and Robinson (1990). Generally,
gleaning involves the simple act of picking or taking a food item
without much effort and without beating; probing involves investigating with the beak and searching for food between the cracks in
trees; tapping (or pecking) is an exploratory strike of the substrate
in an attempt to obtain information about a food item; excavating
involves a more complex action of perforation, force, and agility,
with more conspicuous and intense movements of the head; and
tonguing is a simple projection of the tongue to capture food items
that have already been found.
Anatomical data, presented in Donatelli (2012a, b, c, d), were
compared with methods for obtaining food by various species.
Based on this comparison, the relationship between form and function, i.e., between the specific structure of the jaw apparatus of a
species and its characteristic way of obtaining food, was analyzed.
The results of this analysis were used to address the questions proposed in the description of the study objectives, above.
RESULTS
Anatomical aspects of the jaw apparatus of the Meiglyptini woodpeckers
In addition to the structural differences observed in the
cranial osteology of the Meiglyptini birds (Donatelli, 2012a),
there are a number of other differences that are worth mentioning because of their exclusivity, relative to the degree of
development or other particularity to a group of species. The
following characteristics were noted: 1) there is a thin bone
elevation in the middle portion of the frontal region, named
the frontal overhang by Bock (1999), which is only observed
in H. concretus; 2) the parietal region has nearly 2 ×, 1.5 ×,
and 2.5 × the lateral expansion of the frontal region in H.
concretus, M. pulverulentus and M. tristis and M. tukki,
respectively; 3) the zygomatic process is thick and long in
species from Mulleripicus and short in all other species; 4)
the suprameatic process is only conspicuous in species
from Mulleripicus; 5) the pes pterygoidei is relatively large
in species from Mulleripicus; relatively small, thin and narrow in species from Meiglyptes and inconspicuous in H.
concretus; 6) the fossa choanalis is relatively wide in H.
concretus, followed by Meiglyptes spp. and then Mulleripicus
spp.; 7) the ventral palatine fossa is deep in M. tristis, less
deep in Mulleripicus spp. and shallow in M. tukki and H.
concretus; 8) the ectetmoid projection is relatively short
and thin in Mulleripicus spp., and more developed in H.
concretus; 9) the medial condyle is generally the most
developed element in all of the species, but it is prominent
and pointed in M. tristis; 10) the caudal condyle is an
extension of the lateral condyle in all species; 11) the pars
symphisialis mandibulae is short and slightly more than 1/3
of the total length of the mandible in Meiglyptes spp., while
it is approximately 40% of the total length of the mandible in
M. pulverulentus and nearly 45% of the total mandible
length in H. concretus.
In addition to the structural differences in the components of the mandible musculature in Meiglyptini species
(Donatelli, 2012b), there are a few other notable characteristics: 1) the components of the external mandibular adductor system of H. concretus, particularly the M.a.m.e. caudalis
medialis, are relatively poorly developed compared to other
species; 2) Meiglyptes spp. have a structure that differs
from the other species in terms of certain components of the
external mandibular adductor system (rostralis temporalis,
externus ventralis, caudalis lateralis); 3) the muscles of the
internal mandibular system are relatively poorly developed
in size and structure in H. concretus and are structurally differentiated in Meiglyptes spp.; 4) the M. protractor quadrati
is vestigial in Meiglyptes spp.; 5) the muscles of the protractor system of the quadrate are relatively poorly developed in
H. concretus; 6) most of the muscles of the pterygoideus
system are structurally different in Meiglyptes spp.
The external and internal mandibular adductor system,
the protractor system of the quadrate and the pterygoideus
system in H. concretus are relatively less developed than
in other Meiglyptini species. In Meiglyptes, these components are differentiated from the other species by certain
muscles of the external adductor system, namely M.
pseudotemporalis profundus and M. pterygoideus dorsalis
medialis.
Anatomical aspects of the jaw apparatus of Picini woodpeckers
In addition to the structural differences in the components
of the cranial osteology of Picini woodpeckers (Donatelli,
2012c), there are a number of characteristics noteworthy for
their exclusivity, relative development, or other particularity
in a species, genus or group of species: 1) the parietal/frontal
Jaw apparatus and feeding habit in picids
diameter ratio is typical and relatively large in smaller woodpeckers; 2) the post-orbital process is relatively standard in
Picini woodpeckers (1/3–1/5), except for C. lucidus (4/5); 3)
the pes pterygoidei is a well-developed structure that stands
out in all Picini woodpeckers; 4) the presence of a frontal
overhang differs between the genus Picus and other Picini
members; 5) the orbital process of the quadrate is relatively
larger in B. rubiginosus; 6) the ventral palatine fossa is relatively deep in B. rubiginosus; 7) there is a clear distinction
between species of the genus Picus and other Picini species in relation to the general cranial bone structure; 8) B.
rubiginosus, C. lucidus, R. validus, G. viridis and the other
species of Dinopium have particularities that, based on the
current level of understanding, are too complex to identify
the relationships between them.
In addition to the structural differences in the components of the mandibular musculature of the Picini woodpeckers (Donatelli, 2012d), some characteristics are worth to
mention: 1) in general, the components of the external mandibular adductor system in Picini woodpeckers are relatively
more developed in larger species (e.g., R. validus and D.
rafflesii); 2) there is a clear association between the ventralis
lateralis and dorsalis lateralis adductor muscles by means of
fleshy connecting fibers in all of the species; 3) the jaw musculature of Picus spp. differs from the rest of the Picini members with regards to the poor development of the muscles of
the quadrate protractor system (M. protractor quadrati and
M. protractor pterygoidei); 4) the orbital process of the
quadrate is relatively larger in B. rubiginosus, while the M.
pseudotemporalis profundus is relatively less developed; 5)
the muscles of the pterygoideus ventralis system are more
developed in B. rubiginosus in combination with the greater
relative depth of the ventral palatine fossa in this species; 6)
generally, the M. pseudotemporalis superficialis begins in
Table 1.
225
the ventrocaudal region of the laterosphenoid (lower part of
the pleurosphenoid region), with the only notable exception
being that it begins in the upper part of the pleurosphenoid
region in D. javanense; 7) the M. pterygoideus ventralis
medialis has a third component in D. rafflesii; 8) in addition
to B. rubiginosus, the protractor pterygoidei muscle in D.
rafflesii and D. javanense is more developed than in other
species; 9) in R. validus the protractor quadrati muscle is
relatively more complex, while in the other Dinopium species this muscle is rudimentary; 10) there is a clear difference in the structure of the mandibular musculature
between Picus species and other Picini. B. rubiginosus, C.
lucidus, R. validus, G. viridis, and Dinopium species all
have additional particularities, but given the current level of
understanding, it is difficult to identify relationships among
them.
Food strategies of woodpeckers
According to Short (1982), Winkler et al. (1995) and
Winkler and Christie (2002), Meiglyptini species occupy
arboreal habits and their foraging strategies can be divided
into four categories: 1) gleaning, 2) probing, 3) tapping, and
4) excavating. Most Picini species also occupy arboreal habits, and their principal foraging habits can be divided into five
categories: 1) gleaning, 2) probing, 3) tapping, 4) excavating
and 5) tonguing. Table 1 shows the foraging strategies of
these woodpeckers, the importance of each of these methods for each species, the location where the food items are
found and the type of food consumed by each species.
Jaw apparatus and food strategies
What is the relationship between these feeding parameters and the jaw apparatus? According to the above
results, at least three types of jaw apparatus may be
Methods of obtaining food and types of food of woodpeckers from the Oriental region.
Species
M. pulverulentus
M. tristis
M. tukki
H. concretus
P. miniaceus
P. puniceus
P. mentalis
P. vittatus
P. squamatus
P. viridis
P. canus
D. rafflesii
D. javanense
D. benghalense
C. lucidus
G. viridis
S. noguchii
B. rubiginosus
R. validus
G
T
‫ع‬
‫ع‬
‫ع‬
‫ع‬
‫ع‬
‫غ‬
‫ع‬
‫ع‬
‫غ‬
‫ع‬
‫ع‬
‫ع‬
‫غ‬
‫ع‬
‫غ‬٤
‫غ‬
‫غ‬
‫غ‬
‫ع‬
‫غ‬
‫ع‬
‫غ‬
‫غ‬
‫ع‬
P
E
‫غ‬
٤
‫غ‬٤
‫غ‬
‫غ‬
‫ع‬
‫ع‬
‫ع‬
‫ع‬
‫ع‬
‫غ‬
‫ع‬
‫ع‬
٤
‫ع‬
‫ع‬
‫غ‬
٤
‫ع‬
‫ع‬
‫ع‬
‫ع‬
To
‫ع‬
‫ع‬
‫ع‬
‫غ‬
‫غ‬
Local
Food
trees
trees
trees
trees
trees
trees
trees
ground
both
ground
ground
trees
trees
trees
trees
trees
trees
trees
trees
ants and beetle larvae
ants and other insects
ants and other insects
fruits
ants, eggs and larvae
ants, eggs and termites
ants, termites, beetles
beetles, flies
ants, termites, berries (W)
ants, earthworms, snails, fruits & berries, nectar
ants, earthworms, snails, fruits & nuts, acorn, nectar
ants, termites, pupae
ants, larvae, scorpions
ants, larvae, fruits, nectar
lizards, beetle larvae, ants, pupae, nectar
ants, larvae, beetles
large arthropods, fruits, berries, seeds
beetles, insect larvae
beetle larvae, ants, termites, berries
‫ – ع‬primary or main action; ‫ – غ‬secondary action; ٤ – eventual action.
W – Winter. G – gleaning; T – tapping; P – pecking; E – excavating; To – tonguing.
Categories based on Short (1982), Winkler et al. (1995) and Winkler and Christie (2002).
226
R. J. Donatelli et al.
inferred. 1) Robust, developed and complex: greatest development of the zygomatic, suprameatic, and quadratic processes and of the pes pterygoidei; all of the components
associated with the muscles that act in cranial kinesis; protractor muscles of the quadrate and external mandibular
adductors relatively more developed, which is observed in
M. pulverulentus, whose principal food source is ants, larvae, and beetles; especially the protractor muscles of the
quadrate and external mandibular adductors, as observed in
B. rubiginosus and R. validus, which are primarily excavators that feed on ants, ant larvae and beetles. 2) Poor developed: particularly the protractor muscles of the quadrate and
the external mandibular adductors, as observed in Picus
spp., whose principal foraging strategy is gleaning and who
feed on ants and termites (and beetles, in the case of P.
mentalis). Moreover, the components of the external and
internal mandibular adductor system and of the protractor of
the quadrate system are relatively poorly developed. This is
observed in H. concretus, which feeds on fruits in the tree
canopy. 3) Intermediate type between the previous types, as
observed in Dinopium spp., who glean, probe and tap and
who feed on ants, termites and (secondarily) beetles and
their larvae (D. javanense); particularly with regard to the protractor muscles of the quadrate, external mandibular adductors and muscles of the pterygoideus system; for example,
the M. protractor quadrati is vestigial, and some components of the external mandibular adductor system are differentiated (rostralis temporalis, externus ventralis, caudalis
lateralis). This is observed in Meiglyptes, spp., whose principal food is ants and other insects.
DISCUSSION
In a classic work of interpretation of the development of
the jaw apparatus in relation to feeding habit, Richards and
Bock (1973) associated the cranial bone development and
the musculature that moves the maxillae with the feeding
strategies and food type of Hawaiian honeycreepers from
the genus Loxops (Drepanididae). The authors found that in
species with more robust skulls, the development of the
musculature of the maxillae is greater. Furthermore, the
species that have used this musculature in a less vigorous
way are the same species that have less robust skulls, less
developed maxillary musculature and methods for obtaining
food that require less effort, such as feeding on nectar and
catching insects (gleaning) from leaf surfaces (Richards and
Bock, 1973, p. 79–81). In the same field of research Zusi
(1993) carried out a revision work of the relationship
between the morphology of the skull and functional anatomy; his analysis was based on the different types of bird
cranial kinesis and their roles in the movement of the jaw relative to the braincase. Both classical works are used here
but in a distinct direction: the morphology of the jaw apparatus area related to feeding habits and food source, that is
associated with feeding ecology.
Of the Meiglyptini woodpeckers studied, all are characterized as having arboreal habits. However, they can be divided
into three main foraging categories, according to Short
(1982), Winkler et al. (1995) and Winkler and Christie (2002):
1) gleaning, 2) probing and 3) tapping. According to these
authors, excavating occurs occasionally in M. pulverulentus
and tonguing has not been observed in any Meiglyptini
woodpecker. Furthermore, nothing is known about the feeding behavior of M. fulvus and M. funebris, and this analysis
will be restricted to M. pulverulentus and the other species
of Meiglyptini woodpeckers. Mulleripicus pulverulentus,
Meiglyptes tristis and M. tukki, in addition to H. concretus,
primarily glean to obtain food items, which are mainly ants,
larvae, and other insects (except in the case of H. concretus,
which feeds on fruits). Mulleripicus pulverulentus and H.
concretus use probing and tapping as secondary techniques, but no species of Meiglyptes appears to use probing
or tapping, even as a secondary strategy. Therefore, the primary foraging action of these woodpeckers is gleaning, irrespective of the type of food item consumed. No Meiglyptini
species has a generalist feeding behavior, but some are generalists with regard to type of food. While M. pulverulentus
and the Meiglyptes species search for insects on tree
trunks, H. concretus searches for fruits in the tree canopy.
Smaller woodpeckers, such as M. tristis and M. tukki,
have a more complex jaw apparatus (type 2) and are more
generalist in terms of feeding habit (insects). Mulleripicus
pulverulentus is a specialist and has a relatively complex
mandible (type 1), and it feeds on both ants and beetle larvae. However, this does not justify the distinction in complexity in relation to Meiglyptes spp. The smallest species
(type 3), H. concretus, has a feeding strategy that differs
from the other species, and it only consumes fruits. Based
on this comparison, it is possible that natural selection has
resulted in a more complex structure for birds that capture
insects, and a less complex structure for species that do not
need to capture insects, driven either by ecological (competition) or behavioral (foraging in the canopy of trees) factors.
Either way, it appears that anatomical characteristics of the
jaw apparatus are associated with feeding behavior, feeding
location and competition for food.
With regards to the Picini woodpeckers studied, all of
the species can be characterized as having arboreal habits.
Furthermore, they can be divided into five main foraging categories, according to Short (1982), Winkler et al. (1995) and
Winkler and Christie (2002): 1) gleaning, 2) probing, 3) tapping, 4) excavating, and 5) tonguing. Only P. puniceus has
five primary foraging behaviors. Of these feeding strategies,
some are primary behaviors: a) gleaning and probing (P.
mentalis); b) gleaning, probing and tapping (D. rafflesii and
D. javanense); c) excavating (B. rubiginosus and R. validus);
d) tapping (R. validus); and e) gleaning (P. miniaceus).
Some are secondary behaviors: a) probing and tapping (P.
miniaceus) and b) tapping (P. mentalis). A relationship
between foraging category and type of food taken can also
be observed: 1) P. puniceus feeds on ants and termites and
uses all types of foraging; 2) P. mentalis feeds on a wide
range of food items (ants, termites, crickets, beetles, grasshoppers and even green berries) and uses gleaning and
probing as primary foraging strategies; 3) B. rubiginosus
and R. validus feed on beetles, beetle larvae and ants, and
primarily use excavating; 4) P. miniaceus feeds on ants, and
its principal foraging strategy is gleaning; and 5) D. rafflesii
and D. javanense feed on ants, termites and larvae (except
beetles), and their principal foraging strategies are gleaning,
probing and tapping.
Thus, the primary foraging strategies used by these
woodpeckers are gleaning and probing, followed by tapping,
Jaw apparatus and feeding habit in picids
excavating, and tonguing. The principal food items, independent of foraging mode, are ants (and their larvae), termites,
and beetles.
Picus puniceus is the most generalist species in terms
of foraging strategies and is an ant and termite specialist (as
is P. mentalis). In contrast, P. miniaceus is an ant specialist,
but it primarily gleans. Woodpeckers that primarily glean and
probe have a wide range of food items available to them.
Excavating specialists also consume harder food items such
as beetles (B. rubiginosus and R. validus). Smaller woodpeckers (except for B. rubiginosus) have a less complex jaw
apparatus (type 2), are more generalist in terms of food
items (insects), and use gleaning and probing as their main
foraging strategies. Relatively large woodpeckers (with the
exception of B. rubiginosus) are specialists in terms of food
items and foraging strategies and have relatively complex
mandibles (type 1). Type 3 can be found regardless of size.
The success of woodpeckers as a natural group is due
not only to their feeding diversity but also their wide ability
to explore different resources. Additionally, foraging strategies are related to the diameter, type, conditions and height
of tree trunks for arboreal species and soil type for terrestrial
species (Winkler and Christie, 2002). Furthermore, the jaw
apparatus of oriental woodpeckers is closely related to the
feeding habits and food sources of these species.
ACKNOWLEDGMENTS
The authors are grateful to the Museum Zoologicum Bogoriense,
the Indonesian Institute of Sciences (LIPI), and the Natural History
Museum of the Indonesian Institute of Sciences (MZB), Indonesia,
for loaning him the Picini for anatomical studies. The author also
would like to thank the National Museum of Natural History (USNM),
Smithsonian Institution, Washington DC, USA for allowing him to
visit their collection and study the Picidae.
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(Received July 16, 2013 / Accepted December 22, 2013)